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Tactile Learning by a Whip Spider, <I>Phrynus Marginemaculatus</I

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Tactile Learning by a Whip Spider, <I>Phrynus Marginemaculatus</I University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Eileen Hebets Publications Papers in the Biological Sciences 4-2009 Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch (Arachnida, Amblypygi) Roger D. Santer University of Limerick, Ireland, [email protected] Eileen Hebets University of Nebraska - Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/bioscihebets Part of the Behavior and Ethology Commons Santer, Roger D. and Hebets, Eileen, "Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch (Arachnida, Amblypygi)" (2009). Eileen Hebets Publications. 47. https://digitalcommons.unl.edu/bioscihebets/47 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Eileen Hebets Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 195:4 (April 2009), pp. 393-399; doi: 10.1007/s00359-009-0417-8 Copyright © Springer-Verlag 2009. Used by permission. Submitted October 27, 2008; revised January 12, 2009; accepted January 16, 2009; published online February 7, 2009. Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch (Arachnida, Amblypygi) Roger D. Santer1, 2 and Eileen A. Hebets1 1. School of Biological Sciences, University of Nebraska–Lincoln, Lincoln, NE 68588, USA 2. Department of Life Sciences, Schrödinger Building, University of Limerick, Limerick, Ireland Corresponding author — Roger D. Santer, email [email protected] Abstract The ability of animals to learn and remember underpins many behavioral actions and can be crucial for survival in certain contexts, for example in finding and recognizing a habitual refuge. The sensory cues that an animal learns in such situations are to an extent determined by its own sensory specializations. Whip spiders (Arachnida, Ambly- pygi) are nocturnal and possess uniquely specialized sensory systems that include elongated “antenniform” forelegs specialized for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spi- der Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tac- tile examination. We discuss the potential importance of tactile learning in whip spider behavior and a possible role for their unique giant sensory neurons in accessing tactile information. Keywords: texture discrimination, associative learning, giant neuron, orientation, mechanoreception Abbreviations: CS = Conditioned stimulus; fps = frames per second; GN = Giant neuron Introduction 1998; Collett and Collett 2002). However, environmental features provide sensory cues across many modalities, Learning allows an animal to modify its behavior in and the ones learned and exploited by an animal for the accordance with current environmental conditions. This guidance of its behavior will likely reflect its own sen- ability can be crucial for survival, for example when sory specializations (e.g. Dyer 1998). toxic foods must be avoided after exposure or habitual Whip spiders, non-spider arachnids in the order Am- shelters and/or food sources found and returned to. blypygi, are interesting from this point of view since Many animals that shelter or forage repeatedly in par- they are nocturnal and possess uniquely specialized sen- ticular locations find and recognize these locations (or sory systems highly adapted for the reception of chemo- goals), using strategies that incorporate learned asso- and mechanosensory cues. Walking on only their ciations between the goal itself and sensory cues from posterior three pairs of legs, their first pair of legs (‘an- permanent or reliable environmental features (e.g. Shet- tenniform legs’) are enormously elongated (2.5× their tleworth 1998). For many species, visual and olfactory body length in some species but much longer in others), cues are of particular importance for these purposes and specialized for a sensory function. These antenni- (e.g. Dittman and Quinn 1996; Dyer 1998; Shettleworth form legs are covered with many types of chemo- and 393 394 SANTER & HEBETS IN JOURNAL OF COMPARATIVE PHYSIOLOGY A 195 (2009) mechanosensory sensilla (Igelmund 1987), and contain males and six females) collected from Big Pine Key, at least seven unique giant neurons that carry mechano- FL, USA in August 2006. Whip spiders were individu- sensory information rapidly from these sensilla to the ally housed under a reversed 12:12 hour light cycle in central nervous system (Igelmund and Wendler 1991a,b; 100 mm × 100 mm × 125 mm plastic boxes. Humidity Spence and Hebets 2007). When active, whip spiders was maintained using water-soaked cotton wicks that constantly probe the area around them with their an- also allowed access to water, and whip spiders were tenniform legs both when walking and when stationary fed one cricket twice per week. Experiments were con- (regardless of illumination conditions), and the antenni- ducted in August 2007. form legs are considered the most important structures for spatial orientation (Weygoldt 2000). Experimental arena Many whip spiders reliably inhabit particular ref- uges during the day and return to them after forag- Experiments were conducted in a circular plastic ing at night. Individual Phrynus pseudoparvulus (de Ar- arena with two slits cut in the floor (Figure 1a). A dark- mas and Víquez 2001) occupy particular tree crevices ened 85 mm × 85 mm × 60 mm plastic box was placed or buttresses at the base of trees during the day, but beneath each slit as a refuge. The arena was lit from leave them to forage at night (Hebets 2002); individ- above using a fiber optic lamp (FO-150 “Lumina,” Chiu ual Heterophrynus batesii and H. longicornis reside on Technical Corporation, Kings Park, NY, USA) with a the same tree for weeks or months, occasionally leav- light guide positioned approximately 300 mm above ing the tree to forage at night but returning before dawn each arena floor slit. This strongly illuminated the arena (Beck and Görke 1974; Weygoldt 1977). Whip spiders [1,400 lux, measured using a VWR Scientific dual range can also orient to their refuges when artificially dis- light meter (model 62344-944), West Chester, PA, USA], placed from them: H. batesii displaced up to 10 m from but left each refuge dark. Each refuge was marked with their home tree can navigate back to it, within one night a tactile cue: a 100 mm × 50 mm sandpaper patch sur- for displacements <7.5 m (Beck and Görke 1974; Wey- rounding the slit and a 10 mm × 60 mm sandpaper wall goldt 2000). It has been hypothesized that sensory cues along the side of the slit closest to the arena wall (Fig- (particularly olfactory cues) received by the antenni- ure 1b). Tactile cues were made from aluminum oxide form legs are important in this context since removing sandpaper (Norton Abrasives, Worcester, MA, USA); the distal tips of a whip spider’s antenniform legs pre- one tactile cue had a coarse texture (P36, average parti- vented it from returning to its refuge after being dis- cle diameter 538 μm), the other a fine texture (P400, av- placed (Beck and Görke 1974; Weygoldt 2000). erage particle diameter 35 μm). Tactile cues were spray- Since the antenniform legs of whip spiders are spe- painted flat black (Quick Color Spray Enamel, Roc Sales cialized for the reception of mechanosensory cues as Inc., Vernon Hills, IL, USA) to minimize visual differ- well as chemosensory ones, in this study we wanted to ences between them. After painting, the experimenter investigate whether the whip spider P. marginemaculatus could easily distinguish the different tactile cues on the C. L. Koch is capable of tactile learning. Specifically, we basis of touch. investigated whether this species could learn to associ- ate a tactile proximal cue with a refuge. Individual P. Training trials marginemaculatus are reliably found beneath particular ‘home’ limestone rocks in the pine rock hammock of the During training trials, the entrance to one refuge was Florida Keys during the day, but leave these refuges to accessible and the other was inaccessible (the entrance forage at night (E. A. Hebets, unpublished). These rocks to the inaccessible refuge was covered with a plas- vary in size, shape, and surface texture (R. D. Santer and tic mesh that prevented a whip spider from entering). E. A. Hebets, personal observation). As such, tactile cues Whip spiders were divided into two groups of six (three received by the antenniform legs are a potential source males and three females). For one group the accessible of information that P. marginemaculatus could exploit in refuge was always associated with the coarse textured orienting to, and recognizing its home rock, as well as tactile cue, for the other it was always associated with for the more general guidance of behavior. the fine textured tactile cue. We refer to the tactile cue associated with the accessible refuge as CS+ (CS = con- ditioned stimulus), and the one associated with the in- Materials and methods accessible refuge as CS−. Tactile cues were randomly as- signed a side of the arena for each trial to prevent side We investigated whether whip spiders could learn to effects or external landmarks indicating refuge identity associate a tactile proximal cue with a refuge using aver- or position. sive strong lighting conditions during the dark phase For each whip spider, ten training trials were con- of their light cycle as motivation.
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